Reductive evolution of the DNA replication machinery in endosymbiotic fungi

Abstract

The molecular machinery for replicating and repairing DNA accurately is critically important for life and highly conserved across the Tree of Life. Here we show that two major lineages of fungi, Glomeromycotina and Microsporidia, lost DNA polymerase complexes involved in replication and translesion synthesis. Catalytic and non-catalytic subunits of DNA polymerases are co-eliminated, consistent with their physical and functional interactions described in other eukaryotes. We detect lineage-specific variation in genome-wide mutation rates, showing that DNA polymerase gene losses correlate with increased genetic variation. We find that the Glomeraceae family of arbuscular mycorrhizal (AM) fungi has lived for [~]360 My without a leading strand replisome, raising the question of how these fungi can replicate DNA. We provide evidence that the cell cycle of Rhizophagus irregularis is active when in symbiosis with a host, but not without. This indicates a higher level of integration between AM fungi and plants than previously appreciated, and suggests the existence of a regulatory or functional contribution provided by a host to the fungal cell cycle. We propose that alternative modes of DNA replication and cell cycle provide mutational opportunities for fungal adaptation, and play roles in the evolution of endosymbioses.